Testosterone Related to Age and Life-History Stages in Male Baboons and Geladas
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ARTICLE IN PRESS YHBEH-02887; No. of pages: 9; 4C: Hormones and Behavior xxx (2009) xxx–xxx Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh Testosterone related to age and life-history stages in male baboons and geladas Jacinta C. Beehner a,b,⁎,1, Laurence Gesquiere c,1, Robert M. Seyfarth d, Dorothy L. Cheney e, Susan C. Alberts f,g, Jeanne Altmann c,g,h a Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA b Department of Anthropology, University of Michigan, Ann Arbor, MI 48109, USA c Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA d Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA e Department of Biology, University of Pennsylvania, Philadelphia, PA 19104, USA f Department of Biology, Duke University, Durham, NC 27708, USA g Institute of Primate Research, National Museums of Kenya, Nairobi, Kenya h Department of Animal Physiology, University of Nairobi, Nairobi, Kenya article info abstract Article history: Despite significant advances in our knowledge of how testosterone mediates life-history trade-offs, this Received 26 April 2009 research has primarily focused on seasonal taxa. We know comparatively little about the relationship Revised 11 August 2009 between testosterone and life-history stages for non-seasonally breeding species. Here we examine Accepted 12 August 2009 testosterone profiles across the life span of males from three non-seasonally breeding primates: yellow Available online xxxx baboons (Papio cynocephalus or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or P. h. ursinus), and geladas (Theropithecus gelada). First, we predict that testosterone profiles will track the reproductive Keywords: fi Androgen pro les of each taxon across their respective breeding years. Second, we evaluate age-related changes in Fecal steroid testosterone to determine whether several life-history transitions are associated with these changes. Hormone Subjects include males (N2.5 years) from wild populations of each taxon from whom we had fecal samples Life history for hormone determination. Although testosterone profiles across taxa were broadly similar, considerable Maturation variability was found in the timing of two major changes: (1) the attainment of adult levels of testosterone Method validation and (2) the decline in testosterone after the period of maximum production. Attainment of adult testosterone levels was delayed by 1 year in chacmas compared with yellows and geladas. With respect to the decline in testosterone, geladas and chacmas exhibited a significant drop after 3 years of maximum production, while yellows declined so gradually that no significant annual drop was ever detected. For both yellows and chacmas, increases in testosterone production preceded elevations in social dominance rank. We discuss these differences in the context of ecological and behavioral differences exhibited by these taxa. © 2009 Elsevier Inc. All rights reserved. Introduction that high T facilitates inter-male competition at times in the life cycle when males need to compete for receptive females or the resources The steroid hormone testosterone (T) is known to affect many necessary to attract such females. However, because high levels of T vertebrate life-history traits and has been implicated as a mediator of may interfere with paternal behavior (e.g., Goymann et al., 2007; Gray life-history trade-offs (Hau, 2007; Ricklefs and Wikelski, 2002; et al., 2006; Muller et al., 2009; Nunes et al., 2000, 2001), T levels reviewed in Zera and Harshman, 2001). For example, the increase in should decrease when males care for offspring. Formulation of the production of T when males reach puberty and begin to seek out challenge hypothesis was based on monogamous, seasonal birds with mating opportunities is at the same time associated with costs, such as a high degree of paternal care and cycles of mating and care within reduced immune function (McGlothlin et al., 2007). each year. For such seasonal species with relatively short and intense One model for T-behavior trade-offs, known as the “challenge cycles of mating, the period of interest for investigating T-mediated hypothesis”, proposes that variation in male T across life-history trade-offs is within each breeding season (temperate birds: e.g., stages reflects differential allocation to mating and parenting behavior McGlothlin et al., 2007; Wingfield et al., 1990; tropical birds: e.g., Hau (Wingfield et al., 1990). Specifically, the challenge hypothesis predicts et al., 2008; reptiles: e.g., Wack et al., 2008; and mammals: e.g., Brockman et al., 2001; Cavigelli and Pereira, 2000; Malo et al., 2009; Moss et al., 2001; Ostner et al., 2002, 2008). ⁎ Corresponding author. Department of Psychology, University of Michigan, 530 More recently, the hypothesis has been modified to apply to non- Church St., Ann Arbor, MI 48109-1043, USA. Fax: +1 734 763 7480. E-mail address: [email protected] (J.C. Beehner). seasonally breeding species (Archer, 2006; Muller and Wrangham, 1 Authors Beehner and Gesquiere contributed equally toward this manuscript. 2004). For non-seasonal species, T changes across the year are less 0018-506X/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2009.08.005 Please cite this article as: Beehner, J.C., et al., Testosterone related to age and life-history stages in male baboons and geladas, Horm. Behav. (2009), doi:10.1016/j.yhbeh.2009.08.005 ARTICLE IN PRESS 2 J.C. Beehner et al. / Hormones and Behavior xxx (2009) xxx–xxx informative than T changes across the life span (e.g., Bribiescas, 2006; Although high-dominance rank facilitates reproductive access Crawford et al., 1997; Ellison et al., 2002; Martin et al., 1977). to females in both baboon taxa, behavioral data and paternity Therefore, with respect to T-mediated trade-offs for non-seasonal determination indicate that non-alpha males are thought to be species, T should be up-regulated at the start of reproductive more viable competitors for females in yellow baboon groups than maturity, maintained throughout the breeding years, and down- they are in chacma groups (Alberts et al., 2003, 2006; Bulger, 1993; regulated once males no longer breed or when they focus on paternal Cheney and Seyfarth, unpublished data). Mating in some chacma behaviors. For non-seasonal species, many of the potential trade-offs populations may therefore at any one time be relatively more extend across life-history stages that can take years for long-lived unimale than yellow baboons due to higher reproductive skew. organisms. With the exception of several studies of human and Furthermore, the timing of paternal care for chacma males may captive non-human primates (e.g., Bribiescas, 2001, 2005, 2006; also parallel that described for geladas because (1) paternal care Crawford et al., 1997; Ellison et al., 2002; Martin et al., 1977), serves to protect offspring from infanticide (Palombit et al., 2000), investigation of T profiles across the entire life span is rare (but see (2) infanticidal males are generally newly immigrant males that chimpanzees (Pan troglodytes): Seraphin et al., 2008; and mandrills have attained the alpha position in the dominance hierarchy (Bulger (Mandrillus sphinx): Setchell and Dixson, 2002). and Hamilton, 1987; Busse and Hamilton, 1981; Collins et al., 1984; Here we examine T profiles across the life span of males in wild Palombit et al., 2000; Tarara, 1987), and therefore (3) paternal populations of three long-lived, non-seasonally breeding primate behavior generally occurs after a father has fallen from the alpha taxa (see Methods section): yellow baboons (Papio cynocephalus position. or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or Based on these differences, two predictions emerge. If, as in P. h. ursinus), and geladas (Theropithecus gelada). Specifically, we many bird species (Wingfield et al., 1990), T profiles are linked evaluate age-related changes in T and examine whether several primarily to demographically defined mating systems, gelada T life-history transitions (or “maturational milestones”) are associ- profiles will exhibit a more discrete period of elevation while those ated with these changes. Despite the rarity of mammalian paternal of yellow and chacma baboons will exhibit a more extended period care, baboon and gelada males are known to invest in some degree of adult T levels. Alternatively, if T profiles track the actual differ- of paternal care (Beehner and Bergman, 2008; Buchan et al., 2003; ences among taxa in reproductive access to females and parenting Dunbar, 1984; Moscovice et al., 2009; Palombit et al., 2000). behavior, geladas and chacmas will exhibit a discrete period of T Therefore, we expect that trade-offs between the high levels of T elevation, and yellow males will exhibit a more extended period of optimal for mating and the low levels of T optimal for parenting adult T levels, characterized by a gradual fall in T after peak repro- will result in T modulation for these three taxa, and that this ductive years. modulation will reflect differences among them in their respective Third, we describe the relationship between the maturational rise life histories. in T levels and several male maturational milestones. One visible We have three lines of inquiry. First, as a physiological validation maturational marker, (1) enlargement of testes, is available for only and in accordance with T profiles from other vertebrate species, we one taxon (yellow baboons) and has been shown to precede test the prediction that juvenile males have significantly lower fecal T significant increases in fecal T metabolites (Gesquiere et al., 2005). metabolites than adult males. Further, based on profiles of T across the Therefore, we examine the relationship in these three taxa between T human male life span, T for all three taxa should exhibit an inverse U- profiles and four additional maturational markers: (2) timing of natal shaped pattern, exhibiting a rise at or around maturity and a decline dispersal, (3) acquisition of adult dominance rank, (4) first sexual as the animals senesce.